Review article

Neuropsychology of spatial neglect

A syndrome of spatial attentional spectrum

DOI: https://doi.org/10.4414/sanp.2022.w10094
Publication Date: 17.08.2022
Swiss Arch Neurol Psychiatr Psychother. 2022;173:w10094

Dima Daher, Arnaud Saj

Department of Psychology, University of Montréal, QC, Canada

CRIR/Institut Nazareth et Louis-Braille du CISSS de la Montérégie-Centre, Longueuil, QC, Canada

Summary

There is no consistency in the terms used to refer to the syndrome of spatial neglect, with different terms used to refer to the syndrome as a whole or one of its subtypes. There are hundreds of neglect tools available. However many are not able to differentiate presenting subtypes. It is important for clinicians and researchers to critically evaluate the neglect tools being used for the screening and diagnosis of neglect. The objective of this review is to capture the reported definitions for the subtypes of neglect after stroke and map the range of assessment tools employed for each neglect subtype.

Clinical manifestations

Spatial neglect can be defined as a failure to perceive, process and orient to stimuli in the somatic and extrasomatic space that is contralateral to a focal brain lesion. Importantly, the symptoms of spatial neglect cannot be explained by primary motor or sensory disorders, nor by intellectual disorders [1]. It is a multifaceted cognitive disorder that manifests through different symptoms [2]. The percentage of stroke patients who experience spatial neglect varies widely and ranges from 15% to 85% during the acute stage (<20 days), and 30% to 40% after 3 months [33, 107]. More than 80% of patients screened with a detailed battery show some degree of neglect on at least one measure, and 36% show moderate to severe neglect across several measures [33].

Neglect cannot solely be explained by sensory disturbances, as impairments of perceptual processing are also noted in people with neglect. In the acute phase of the disorder, patients show a reproducible ipsilesional deviation of the head and eye [1]. Moreover, they may respond to stimuli coming from the contralesional side as if it was coming from the ipsilesional side [2]. Perceptual extinction is another symptom that cannot be explained by sensory disturbance and is present 23% of the time [111]. When two stimuli are presented simultaneously on each side, the stimulus on the contralesional side is not perceived. However, the same stimulus on the contralesional side is perceived when presented alone. The inability to orient to the contralesional side when presented with a competing stimulus in the intact side can be interpreted as a deficit in spatial attention [3–5] and is present 70% of the time [111].

Motor deficits are associated with spatial neglect and have an incidence of 33% [112]. Multiple studies have tried to distinguish motor deficits from perceptual deficits using different techniques. For instance, in a study by Husain et al. [6] participants had to move their hand, starting from different positions, to respond to a target light appearing on the right or left of a central fixation point. The findings of this study, coupled with findings from other similar studies [7, 8], suggest that patients with neglect may fail to initiate movements in the contralesional area in addition to failing to perceive contralesional visual stimuli. This symptom has been called “premotor neglect” [7]. Another aspect of motor neglect affects the limbs of patients with neglect and is termed “unilateral hypokinesia” [9]. This symptom is characterised by a reduction in spontaneous use and movement of the contralesional limb, without the presence of limb paralysis or weakness [10].

The complex and heterogeneous nature of spatial neglect arises not only from the multisensory modality of the disorder [11], as discussed above, but also from the different reference frames and sectors of space [1]. Moreover, adding to the complexity of the disorder, neglect can affect the mental representation of objects. This deficit can be measured using mental imagery tasks such as asking individuals to describe from memory elements of a familiar place or objects. Neglect patients may omit certain elements in the contralesional side of the setting or object [12].

Different frames of reference can define spatial neglect when left-right coordinates are considered. The contralesional portion of space that is neglected varies between different tasks and stimuli, and between patients. This frame of reference is defined as “egocentric” because it is relative to the midline of the body or head of the individual [108]. Studies have shown that individuals exhibit a biased perception of “straight ahead” by orienting to the right as a default position for their head [13, 14]. Neglect can also affect the left side of each individual object, regardless of their egocentric localisation. This frame of reference is defined as “allocentric” because it is object-centred neglect. Patients may eat food from one side of the plate, shave and apply cosmetics to one side of the face [15]. Moreover, patients may neglect letters during reading and spelling of words [16, 17]. Multiple studies have examined object-centred neglect by manipulating the orientation and nature of the stimulus presented [18–20]. Patients show worse neglect for the left side of an object presented in the right visual field than for the right side of an object presented in the left visual field, which shows the allocentric frame of reference of neglect.

Neglect can selectively affect different sectors of space that can be divided into personal, peri-personal and extra-personal space. The neglect of personal space is defined as the failure of the patient to investigate the contralesional half of their body [21]. To assess personal neglect, patients may be asked to use common objects such as combs, eyeglasses and razors. The symmetry of the task is assessed to determine the severity of personal neglect [22]. The neglect of peri-personal space is a deficit that concerns stimuli present within reaching distance of the patient. Peri-personal neglect is assessed using paper and pencil tasks that evaluate motor, perceptual and selective attention skills such as letter cancellation tests, barrage test and sentence reading test [1, 22, 23]. The neglect of extra-personal space affects stimuli that are present outside reach and in far space. Extra-personal neglect can be assessed using room descriptions and having patients utilise tools [24]. Each of these three subtypes is rarely seen alone, with personal and extra-personal neglect being the most frequent subtypes [22].

There are other types of neglect that are less evaluated and not as common. These include representational deficits and auditory neglect. Neglect of representational space was studied by Bisiach and Luzatti [113]. In their study, participants with visual neglect were asked to describe, from memory, a square in Milan. Consistent with visual neglect symptoms, the participants described the right side of the square and neglected to describe the left side. They were then asked to “turn around” in their mind and describe the square from the other side. This time, the participants were able to describe what had previously been to their left and neglect what was previously on their right. This demonstrates that long-term memory and mental representations are also affected in visual neglect. Auditory neglect is the inattention to stimuli that is presented on the controlesional space [114]. It is assessed by presenting the participant with two simultaneous verbal auditory stimuli in both ears, and then asking the participant to specify the best perceived stimulus. Auditory neglect is usually observed after lesions in the anterolateral parabelt and inferior parietal cortex, or the “where” pathway of the auditory cortex. It is also observed after lesions in the caudolateral parabelt and temporal cortex, or the “what” pathway [115].

It is worth noting that it is important to differentiate between visual neglect and hemianopia, a visual field defect. Hemianopia occurs from lesions to the optic tract and/or striate cortex and causes impairments to the primary perception of contralesional visual information [25]. Typically, patients who have hemianopia can still normally orient towards the contralesional side and do not present the same difficulties that neglect patients encounter in drawing and cancellation tasks. Whilst neglect patients exhibit a graded pattern of deficit from the impaired to the intact side, hemianopia patients display a sharp demarcation between the two sides [1]. However, it is sometimes difficult to differentiate between visual neglect and hemianopia [26, 27]. Although both deficits often occur independently of one another, neglect has been found to mimic hemianopia in severe cases. This “pseudo-hemianopia” is characterised by a complete failure to perceive stimulation in the contralesional visual field that cannot be explained by lesions in the optic tract or striate cortex [26].

Clinical assessment of spatial neglect 

Spatial neglect can be described as highly heterogenous in its clinical manifestations and neuroanatomical correlates. The dissociations in symptom manifestations can be explained by different lesion sites and brain networks associated with neglect [28, 29]. These different aspects of the multi-component disorder are not always overtly evident and batteries that include several different tests are needed to measure and reveal their presence [30]. The observed dissociation in clinical symptoms can be traced back to the various domains affected by visual neglect. Using a factorial analysis, the study by Verdon et al. [28] revealed three main domains that explain 82% of the total variance across all neglect tests. Those three domains are related to the perceptive/visuo-spatial, exploratory/visuo-motor, and allocentric/object-centred aspects of spatial neglect. In this article, we chose to use Verdon’s factorial analysis to classify the various tests used to assess visual neglect under one of those three different domains.

 Perceptive and visuo-spatial component

Perceptive and visuo-spatial aspects of neglect refer to the ability to shift attention spontaneously to the contralesional side and maintain a stable attentional perception of the world over time and despite frequent eye movements that shift the location of objects [28, 31]. Patients demonstrate unilaterally reduced attention and the visuo-spatial neglect symptoms are usually the most obvious and the most impacted by neurorehabilitation [32]. Tasks that usually require little voluntary attentional and motor control are associated with the perceptive and visuo-spatial component of neglect [33]. In Verdon et al. [28] and the factorial analyses of Azouvi et al. [33] , this component was associated with reading, line bisection, clock drawing and identification of overlapping figures tasks that require visual scanning in a systematic manner. Reading tasks and line bisection tasks correlated the most with the perceptive and visuo-spatial component, with factor loadings of 0.87 and 0.86, respectively [28]. Recent studies have been increasingly looking at the correlation between performance in specific tests and different locations of cerebral lesions [34]. The perceptive and visuo-spatial aspect of neglect has been associated with lesions in the right inferior parietal lobule [28], which was long considered to be the only neuropathological correlate of neglect. Supporting this finding, multiple studies have used line bisection tasks to assess parietal function and the perceptive and visuo-spatial aspect of neglect and have found neglect to be associated with posterior parietal damage [35, 36], near the supramarginal gyrus [37]. Damage to the inferior parietal lobe of the posterior parietal cortex has been associated specifically with the perceptual, egocentric and exploratory components of neglect [38]. The representations of perceptual locations within parietal structures helps to promote the maintenance of previously explored locations in spatial working memory [116] and play a critical role in the spatial representations that are necessary to shift attention to contralesional locations. The spatial memory and the attention shifting are two abilities that usually impaired in neglect patients and could potentially be important in pinpointing the endpoints of a line or when returning to the next line in a text [28]. Overall, considering the lower factor loading (0.48) of drawing tasks [28], and previous literature on the link between performance on reading and line bisection tests and damage to posterior parietal cortex, we will consider those tasks as primary tools used to assess the perceptive and visuo-spatial component of neglect.

Reading tasks are used to assess neglect dyslexia, a symptom of spatial neglect where patients present with reading errors in the contralesional side of the text stimulus [39]. Various aspects of neglect dyslexia are reported, such as viewer-centred, stimulus-centred or word-centred neglect dyslexia and can present in multiple spatial scales [16]. Patients with neglect dyslexia might omit text on the entire left page of a book, a left text column, the left side of sentences or left letters in a word. The majority of reading tests used to assess neglect dyslexia are word-level assessments. Such tests might not give an accurate representation of the challenges faced by patients with neglect who encounter more than single words in isolation, in the real world [17]. A more recent study by Galleta et al. [39] used a functional reading task that reflects everyday world reading such as articles and menus. Their findings suggest that functional reading tasks are better at measuring neglect dyslexia severity than word-level assessments.

Line bisection tasks are some of the most commonly used pencil-and-paper tests to assess spatial neglect [2, 40]. Line bisection tasks are easy to administer, are less time-consuming than other tests, have a relative test sensitivity that ranges from 41.67% to 76.4% for spatial neglect and are therefore extensively used in clinical settings [41]. In the standard version of the task, patients are asked to mark the middle of a series of horizontal lines of different lengths with the centre of the lines aligned with the midsagittal plane of the individual’s body [38]. Different versions of this task use different line length and number of lines. For instance, in the version of Schenkenberg et al. [42], 20 lines are used in a random arrangement with some on the right, some in the centre and some on the left of a piece of paper. The lines are 100, 120, 140, 160, 180, and 200 mm in length [40, 42]. In the version of Azouvi et al. [33], four lines 5 cm and 20 cm in length are used and are presented separately. Patients with spatial neglect set their mark with a rightward deviation, toward the ipsilateral end of the line [38]. Typically, the error is more pronounced for longer lines [43, 44]. Studies have shown that judging the left half of the line as shorter implies that the patient experiences a perceptual underestimation of contralateral extent and, therefore, this test has been shown to be effective in measuring the perceptive and visuo-spatial aspects of neglect [38, 45]. The landmark test [46] is a variant of the line bisection task that does not involve a motor response from the patient. It requires the individual to voice which half of a pre-bisected lines is longer or shorter [38]. Other line bisection tasks do not allow the distinction between the motor and the perceptual output, whereas the landmark test has been proven to be effective in separating those two components of spatial neglect [47].

Secondary tools used to assess the perceptive and visuo-spatial component of neglect include tasks mentioned by Verdon et al. [28] and the factorial analyses of Azouvi et al. [33], such as drawing tasks and the identification of overlapping figures test. On the basis of the lower factor loading (0.48) of drawing tasks [28], it was added as a secondary tool to access the visuo-spatial component of neglect. Additionally, a study by Chechlacz et al. [48] found an association between neglect, measured using a cancellation task, and damage to the right supramarginal gyrus, the intraparietal sulcus, the middle frontal gyrus and the superior temporal gyrus. These areas of the brain also correlate with this component of neglect [28]. The target cancellation task was used to identify the visuo-spatial network in awake craniotomies and prevent neglect postoperatively. This task proved to be useful in identifying visuo-spatial cortical and subcortical regions. However, target cancellation tasks do not solely target the interpretation of visual information, they also involve motor functions and therefore stimulation of the motor cortex. Thus, target cancellation tasks may not exclusively assess the visuo-spatial component of neglect and can also measure other components of neglect such as the motor component [49]. This applies to other tasks used to assess visual neglect. Owing to the nature of most of them, they target multiple areas of the brain, and thus assess multiple components of neglect. Very recently, virtual reality tools have been implemented in the assessment of visual neglect. this offers conditions closer to everyday life situations and detects more subtle symptoms of neglect that are not revealed by pencil and paper tasks [85]. Moreover, it ­addresses the limitations of paper and pencil tasks ­because it has better ecological validity, and it offers an environment closer to real-life situations [117].

Exploratory and visuo-motor component

The exploratory and visuo-motor aspects of neglect can be defined as the ability to direct attention and the motor skills used to perform a spatial neglect task [28]. In Verdon et al. [28] and the factorial analyses of Azouvi et al [33], this component was associated primarily with errors in cancellation tests including the Bells and Ota search tasks, and secondarily with errors in drawing tasks, such as landscape copy, reading tasks and line bisection tasks. Ota search and Bells cancellation tasks correlated the most with the exploratory and visuo-motor aspects of neglect, with factor loadings of 0.79 and 0.95, respectively. The landscape copy correlated to a lesser degree with the component, with a factor loading of 0.41 [28]. This component of neglect has been associated with right dorsolateral prefrontal cortex lesions. Regarding the exploratory aspect of the component, spatial neglect caused by right frontal lobe lesions is captured more prominently using cancellation and search tasks that include distractors. Frontal damage has been found to cause more severe attention biases in cancellation and search tasks than other lesions in the brain [50]. Moreover, the deficits noted on drawing tasks may be caused by the patient getting distracted by elements on the right side of the test display [51]. The attention problems and distractions could be explained by the essential role of the dorsolateral prefrontal cortex in the selection of target information and the inhibition of irrelevant distractors during search tasks [118]. Regarding the visuo-motor aspect of the component, damage to the frontal lobe and to the premotor cortex may cause deficits in motor planning as shown in line bisection, cancellation and drawing tasks [52]. Two peaks of frontal damage were noted using a voxel-based lesion-symptom mapping approach [28]. Both peaks were found to be involved in spatial attention and oculomotor control [30, 53]. Thus, dorsolateral prefrontal cortex lesions that cause deficits measured by cancellation, drawing and line bisection tasks, suggest attention and visuo-motor problems when exploring the contralesional space in a task. Moreover, pure motor neglect symptoms that affect the contralesional limbs without affecting the perception often arise after focal lesions in the anterior-lateral thalamus or the medial prefrontal cortex [119, 120]. Overall, on the basis of previous literature and the factorial analysis by Verdon et al. [28], cancellation tasks can be considered primarily tools to assess the exploratory and visuo-motor aspects of neglect, and drawing, reading, line bisection and eyetracking during free exploration tasks [121] can be considered secondary tools.

Cancellation tasks come in multiple versions. Generally, patients are asked to strike target items presented on a piece of paper [38]. In some versions of the tests, including the Bells task [54], several distracters are included amongst the targets. For example, in the Broken Hearts [55] or Circles test [56, 57], participants must mark completely shaped hearts or circles that are intermingled among distractor hearts or circles with gaps on the right or left side of the shape. In other versions of the tests, only targets are presented, such as in the line crossing test [58]. Tasks that include distracters are more effective at detecting neglect than tasks with only targets [59]. Cancellation tasks are scored by counting the total number of errors and the difference between the number of errors on the left- and right-hand sides of the test sheet. Cancellation tasks necessitate active exploration of the test sheet and patients must constantly shift attention between the different items on the piece of paper [60]. The Center of Cancellation developed initially by Binder and al. [131] and more recently Rorden and Karnath [132] provides an intuitive, continuous and robust measure of neglect severity. Patients with neglect with motor-exploratory deficits generally show neglect symptoms on the egocentric reference frame. They may, for example, eat food from plates that are on the right side of their body. Similarly, patients with motor-exploratory deficits will only detect targets on the right-hand side of the page on the cancellation task and will display a right-to-left horizontal scanning pattern that is consistent with exploratory, visuo-motor and egocentric deficits in neglect [61]. Patients with allocentric neglect exhibit different patterns on cancellation tasks, as discussed in the subsequent section.

Secondary tools used to assess the exploratory and visuo-motor aspect of neglect include drawing, reading, line bisection and eyetracking during free exploration tasks. Errors on drawing tasks may be caused by ­attention deficits that lead to the patient getting distracted by elements on the right side of the display and failing to explore the contralateral side [51, 28]. In this task, patients must draw a copy of a figure presented to them or from memory. The figures vary in complexity depending on the test used and more complex drawing tasks are more sensitive to neglect [1]. Some tasks include multiple figures to draw and patients with egocentric neglect fail to reproduce objects on the left-hand side of the paper. Moreover, drawing from memory tasks can provide information about visuomotor deficits. For instance, patients with left neglect will usually only draw on the right-hand side of the paper sheet [38]. Reading requires visuomotor and exploratory skills. Reading material encountered in real life situations, such as articles or menus, are more sensitive than word and phrase reading tasks in measuring spatial neglect. They involve left-to-right scanning which taps into exploratory skills and therefore are more efficient at detecting exploratory deficits [39]. Line bisection tasks and especially the version of Schenkenberg et al. [42] is the most sensitive when assessing the exploratory and visuo-motor aspect of neglect. It consists of three groups of lines, with one group drawn on the left, one in the center and one on the right-hand side of the sheet of paper [62]. The placement of those lines makes for a wide interactive field that is useful in detecting spatial exploration deficits [63]. ­Finally, eyetracking during free visual exploration is performed by testing the sensitivity of eye movement measurement while participants freely explore images of natural scenes or urban places [221]. This task aims to detect neglect in everyday behaviour. The study by Kaufmann et al. [221] found that this task detects significantly more patients with neglect than paper and pencil tasks. Overall, cancellation, drawing and line bisection tasks are the main tools that measure the exploratory and visuo-motor aspects of neglect [64].

Allocentric and object-centred component:

The third and final component of neglect is the allocentric and object-centred aspect that involves one side of the object in regard to its spatial coordinates [38]. It contrasts with the first two components, which both involve space based (egocentric) aspects [28]. Egocentric and allocentric symptoms can co-occur but can also manifest separately. Some studies suggest that those two aspects of neglect are independent [65, 66], but other studies argue that the two frames of reference are essentially egocentric [67, 68]. In the factorial analyses fo Verdon et al. [28], this component was associated mainly with allocentric errors on the Ota search task, with a factor loading of 0.9, and the compound word reading task, with a factor loading of 0.89. This component of neglect has been associated with right temporal lobe lesions [28]. Temporal lobe lesions associated with allocentric neglect have been found to be more ventral than those associated with egocentric neglect [69]. Another recent study by Pedrazzini et al. [60] has demonstrated that damage to the intraparietal cortex is a predictor of allocentric neglect but not egocentric neglect. Their findings suggest that the two frames of reference have distinct underlying processes that are nonetheless interdependent. Moreover, multiple studies found that even though the ventral stream of the temporal lobe is important for coding object shape, it also interacts with the dorsal stream of the parietal cortex, which is involved in the spatial coordinates of object representation and structure [70, 71]. For instance, the parietal cortex is involved in the mental transformation of objects such as rotating them [72]. Furthermore, a meta-analysis by Chechlacz et al. [73] found an association between allocentric symptoms and posterior lesions in the angular gyrus of the inferior parietal lobule. The studies mentioned above that examine allocentric neglect used different tests such as drawing, cancellation, single-word reading, and line bisection tasks. Overall, on the basis of previous literature and the factorial analysis by Verdon et al. [28], cancellation and single-word reading tasks would be considered primarily tools to assess the allocentric and object-centred aspect of neglect, and line bisection and drawing would be considered secondary tools.

Certain versions of the cancellation task can distinguish between allocentric and egocentric neglect [56, 74]. In the study of Verdon et al. [28], Ota’s search task was used and allocentric neglect was measured by counting the omissions of targets with gaps on their contralesional side regardless of their location on the test sheet. When measuring egocentric neglect, the test is scored by counting the number of errors on the contralesional part of the test sheet [1]. In another version of the cancellation task, targets are grouped into two different clusters in such a way that they form two large targets made of smaller targets. Allocentric neglect is measured by counting omissions of targets on the contralesional part of each cluster, while egocentric neglect is measured by counting omissions on the contralesional part of the test sheet [74]. Finally, figurative discrimination tasks such as the Apple cancellation task and the Sensitive Neglect Test [75, 110] are more specialised at assessing both allocentric and egocentric neglect in one test and distinguishing between the two frames of reference [76]. In real word settings, this allocentric neglect may translate into eating food on the right side of each plate while still attending to plates on both sides of the body [61, 78].

Multiple studies have confirmed the efficacy of single-word reading in measuring allocentric neglect [70, 71, 79]. In single-word reading tasks, patients are asked to read right-side-up and upside-down words placed in the centre of a page [61, 80]. Typically, left-sided omissions and substitutions of letters, regardless of the modality, order of presentation and spatial location, are the types of errors seen when measuring allocentric neglect by using single-word reading [1, 61]. Single-word reading requires allocentric processing because single target parts have to be integrated to identify the whole word [60].

Secondary tools used to assess the allocentric aspect of neglect include line bisection and drawing tasks. In line bisection tasks, patients with neglect will mark the line far right of the centre [61]. This error might be the result of neglect of the left half of the body (egocentric) or left half of the object, in this case, the line [81]. To distinguish between the two frames of reference, smaller lines of 5 cm length can be used to assess allocentric neglect. The smaller line may be more precise in helping view the line as an object regardless of its location on the test sheet. Moreover, line bisection tasks can be combined with other tasks such as cancellation tasks to distinguish between the two types of neglect [61]. A study by Golay et al. [82] found that a patient with allocentric neglect shows impairment in line bisection tasks but not cancellation tasks, whereas patients with egocentric neglect demonstrate impairment on cancellation tasks but not line bisection tasks. On a neuroanatomical level, the errors observed in line bisection tasks have been suggested to be due to the activation of the allocentric ventral visual system [83]. Overall, line bisection tasks require object-based processing because the dimension of the line has to be judged [60]. Copying and drawing tasks can measure both allocentric and egocentric neglect [1]. An individual with neglect may fail to reproduce objects on the left-hand side of the paper (i.e., egocentric neglect), as previously discussed [38], but also fail to reproduce the left-hand side of each object (i.e., allocentric neglect). Overall, cancellation, single-word reading, drawing and line bisection tasks require object-based processing and are all important tools to measure the allocentric aspect of neglect [60].

Treatment of spatial neglect 

We can distinguish between three main types of interventions: behavioural rehabilitation, noninvasive brain stimulation techniques and neurofeedback techniques. Behavioural rehabilitation techniques include pencil and paper tasks and more recently virtual reality (VR). Such an approach is called a top-down approach because it targets the individual’s higher level cognitive processes by aiming to correct the perceptual and behavioural biases [84]. Some of the most common tests used are drawing, digit detecting, reading, visual exploration and writing. During those tests, visual scanning training is used, and the patient is instructed to explore the contralesional portions of space [29]. Very recently, VR tools have been implemented in the rehabilitation of visual neglect. It offers conditions closer to everyday life situations and detects more subtle symptoms of neglect that are not revealed by pencil and paper tasks [85]. Moreover, it offers the possibility to control for head, eye, limb and postural movements [86]. Some VR tasks incorporate the use of serious games and immersive virtual reality to enhance training motivation in people with visual neglect [117, 122]. Multiple studies have used VR and compared it with patients undergoing pencil and paper training and found great improvement inn visual neglect assessment tasks, such as cancellation tests, compared with the control group, but also decreased visuo-spatial deficits and improved daily life activities [87-90]. Moreover, a study by Knobel et al. [122] found that VR tasks that incorporate the use of games and immersive virtual reality were rated as a motivating and entertaining tasks, and can be used by different populations with different levels of skills, including individuals with cognitive impairments. Using VR systems may prove to be essential in visual neglect rehabilitation [91].

Noninvasive brain stimulation or neuromodulator techniques include caloric vestibular stimulation (CVS), galvanic vestibular stimulation (GVS), transcranial magnetic stimulation (TMS), transcranial direct current stimulation (tDCS), prismatic adaptation (PA), and optokinetic stimulation (OKS). In CVS, water irrigators are used to cool the contralesional auditory canal or warm the ipsilesional one. This procedure elicits horizontal nystagmus and has shown benefits in treating visual neglect [92]. GVS is a noninvasive procedure that requires application of a weak direct percutaneous current to stimulate the vestibular system [29]. TMS is a procedure that uses magnetic fields to stimulate nerve cells in the brain. Research has shown significantly higher cortical excitability in neglect patients compared with healthy controls. This degree of excitability can be reduced by TMS [123, 124]. In fact, studies have suggested that using inhibitory TMS on the intact left parietal cortex can reduce the left hemisphere activity, which rebalances interhemispheric activity and improve visual neglect symptoms [93–95]. More recently, continuous theta burst stimulation has been introduced as a new protocol. It has inhibitory effects on brain activity and can induce long-term depression in patients with neglect [125]. This protocol leads to significantly longer inhibitory effects on neglect symptoms than TMS and it helps improve and accelerate neglect recovery [126]. Moreover, recent studies have looked at the efficacy of using tDCS on neglect patients. Most of them found an improvement in activities of daily living when inhibitory and excitatory stimulation were used on the left and right posterior parietal cortex, respectively [96–98]. Prismatic adaptation is a technique that consists in producing a visual shift by making the patient wear prismatic googles and take part in different tasks [29]. This procedure has had mixed results, with some studies demonstrating its effectiveness [99] and some finding no beneficial outcomes [100, 101]. This effectiveness seems to be dependent on the location of the lesion [102] but also on the type of task [103]. Finally, optokinetic stimulation (OKS) is a sensory stimulation technique that helps modulate many facets of visual neglect. It leads to the activation of multiple brain regions such as the temporo-parietal cortex and the basal ganglia that are involved in visual space coding [127].

More recently, neurofeedback techniques have been used, a patient can learn to voluntarily control brain activity by learning mental strategies. In a recent paper [104], the authors show that patients with visual neglect were taught how to increase their right primary visual cortex activity using neurofeedback in functional magnetic resonance imaging (fMRI) [105] or with the electroencephalogram (EEG), the acute or chronic patients' improvement in visuo-spatial performance on tests, seem to be very promising [104].

Conclusion

Visual neglect is a complex cognitive disorder that involves multiple factors which can be grouped into three major domains: the perceptive and visuo-spatial, the exploratory and visuo-motor, and the allocentric and object-centred aspects. These three domains correlate with different lesion sites in the brain network [29], that lead to different clinical manifestations that are captured by various tasks. Ideally, multiple assessment tests should be used to fully capture the complex nature of the multi-component syndrome and the various symptoms that may manifest in association or in isolation [38]. Some of the most important tests that should be routinely used include Schenkenberg’s line bisection test [42], target cancellation tasks such as the Bell’s Test [54] or Ota’s search task [56], and drawing tasks such as the Clock Drawing Test [106]. The future evaluation should include VR [128] but also with the EEG [129,130]. Concerning the future of rehabilitation, three main types of interventions are available to treat visual neglect: behavioral rehabilitation, noninvasive brain stimulation techniques and neurofeedback techniques. VR tools are very promising to treat visual neglect have because they offer conditions closer to everyday life situations and are accessible for people with cognitive impairments. More research needs to be done on the efficiency of VR therapy. Overall, considering the multi-factorial and complex nature of this disorder that affects the spatial attention of the patient, we deem it accurate to speak of a spatial attentional spectrum when referring to the syndrome.

Appendix

fullscreen
Table S1

Weight of different neuropsychology tests used to assess the three domains of visual neglect.*

Disclosure statement

No financial support and no other potential conflict of interest relevant to this article was reported

Correspondence

Prof. Arnaud Saj, PhD

Université de Montréal

1700 Rue Jacques-Tétreault

Laval, QC H7N 0A5

Canada

arnaud.saj[at]umontreal.ca

References

1. Vuilleumier P, Saj A. Hemispatial neglect. The behavioral and cognitive neurology of stroke. 2013 Feb 28:126-57.

2. Checketts M, Mancuso M, Fordell H, Chen P, Hreha K, Eskes GA Current clinical practice in the screening and diagnosis of spatial neglect post-stroke: findings from a multidisciplinary international survey. Neuropsychol Rehabil. 2021 ;31(9):1495–126. PubMed

3. Làdavas E. Selective spatial attention in patients with visual extinction. Brain. 1990 Oct;113(Pt 5):1527–38. http://dx.doi.org/10.1093/brain/113.5.1527 PubMed

4. Vuilleumier PO, Rafal RD. A systematic study of visual extinction. Between- and within-field deficits of attention in hemispatial neglect. Brain. 2000 Jun;123(Pt 6):1263–79. http://dx.doi.org/10.1093/brain/123.6.1263 PubMed

5. Di Pellegrino G. Clock-drawing in a case of left visuo-spatial neglect: a deficit of disengagement? Neuropsychologia. 1995 Mar;33(3):353–8. http://dx.doi.org/10.1016/0028-3932(94)00106-Y PubMed

6. Husain M, Mattingley JB, Rorden C, Kennard C, Driver J. Distinguishing sensory and motor biases in parietal and frontal neglect. Brain. 2000 Aug;123(Pt 8):1643–59. http://dx.doi.org/10.1093/brain/123.8.1643 PubMed

7. Bisiach E, Geminiani G, Berti A, Rusconi ML. Perceptual and premotor factors of unilateral neglect. Neurology. 1990 Aug;40(8):1278–81. http://dx.doi.org/10.1212/WNL.40.8.1278 PubMed

8. Coslett HB, Bowers D, Fitzpatrick E, Haws B, Heilman KM, COSLETT HB. BOWERS D, Fitzpatrick E, HAWS B, HEILMAN KM. Directional hypokinesia and hemispatial inattention in neglect. Brain. 1990 Apr;113(2):475–86. http://dx.doi.org/10.1093/brain/113.2.475

9. Valenstein E, Heilman KM. Unilateral hypokinesia and motor extinction. Neurology. 1981 Apr;31(4):445–8. http://dx.doi.org/10.1212/WNL.31.4.445 PubMed

10. Sampanis DS, Riddoch J. Motor neglect and future directions for research. Front Hum Neurosci. 2013 Mar;7:110. http://dx.doi.org/10.3389/fnhum.2013.00110 PubMed

11. Jacobs S, Brozzoli C, Farnè A. Neglect: a multisensory deficit? Neuropsychologia. 2012 May;50(6):1029–44. http://dx.doi.org/10.1016/j.neuropsychologia.2012.03.018 PubMed

12. Bartolomeo P, D’Erme P, Gainotti G. The relationship between visuospatial and representational neglect. Neurology. 1994 Sep;44(9):1710–4. http://dx.doi.org/10.1212/WNL.44.9.1710 PubMed

13. Karnath HO, Rorden C. The anatomy of spatial neglect. Neuropsychologia. 2012 May;50(6):1010–7. http://dx.doi.org/10.1016/j.neuropsychologia.2011.06.027 PubMed

14. Kapoor N, Ciuffreda KJ, Suchoff IB. Egocentric localization in patients with visual neglect. Visual & Vestibular Consequences of Acquired Brain Injury. Santa Ana: Optometric Extension Program. 2001:131-44.

15. Bisiach E. Unilateral neglect and related disorders. InHandbook of clinical and experimental neuropsychology 1999 (pp. 479-496). Psychology Press.

16. Caramazza A, Hillis AE. Levels of representation, co-ordinate frames, and unilateral neglect. Cogn Neuropsychol. 1990 Nov;7(5-6):391–445. http://dx.doi.org/10.1080/02643299008253450

17. Vallar G, Burani C, Arduino LS. Neglect dyslexia: a review of the neuropsychological literature. Exp Brain Res. 2010 Oct;206(2):219–35. http://dx.doi.org/10.1007/s00221-010-2386-0 PubMed

18. Behrmann M, Moscovitch M. Object-centered neglect in patients with unilateral neglect: effects of left-right coordinates of objects. J Cogn Neurosci. 1994;6(1):1–16. http://dx.doi.org/10.1162/jocn.1994.6.1.1 PubMed

19. Driver J, Baylis GC, Goodrich SJ, Rafal RD. Axis-based neglect of visual shapes. Neuropsychologia. 1994 Nov;32(11):1353–65. http://dx.doi.org/10.1016/0028-3932(94)00068-9 PubMed

20. Savazzi S, Mancini F, Veronesi G, Posteraro L. Repetita iuvant: Object-centered neglect with non-verbal visual stimuli induced by repetition. cortex. 2009 Jul 1;45(7):863-9.

21. Beschin N, Robertson IH. Personal versus extrapersonal neglect: a group study of their dissociation using a reliable clinical test. Cortex. 1997 Jun;33(2):379–84. http://dx.doi.org/10.1016/S0010-9452(08)70013-3 PubMed

22. Spaccavento S, Cellamare F, Falcone R, Loverre A, Nardulli R. Effect of subtypes of neglect on functional outcome in stroke patients. Ann Phys Rehabil Med. 2017 Nov;60(6):376–81. http://dx.doi.org/10.1016/j.rehab.2017.07.245 PubMed

23. Pizzamiglio L, Judica A, Razzano C, Zoccolotti P. Toward a comprehensive diagnosis of visual-spatial disorders in unilateral brain damaged patients. Eval Psicol. 1989.

24. Zoccolotti P, Antonucci G, Judica A. Psychometric characteristics of two semi-structured scales for the functional evaluation of hemi-inattention in extrapersonal and personal space. Neuropsychol Rehabil. 1992 Jul;2(3):179–91. http://dx.doi.org/10.1080/09602019208401407

25. Saj A, Honoré J, Braem B, Bernati T, Rousseaux M. Time since stroke influences the impact of hemianopia and spatial neglect on visual-spatial tasks. Neuropsychology. 2012 Jan;26(1):37–44. http://dx.doi.org/10.1037/a0025733 PubMed

26. Kooistra CA, Heilman KM. Hemispatial visual inattention masquerading as hemianopia. Neurology. 1989 Aug;39(8):1125–7. http://dx.doi.org/10.1212/WNL.39.8.1125 PubMed

27. Vallar G, Bottini G, Sterzi R, Passerini D, Rusconi ML. Hemianesthesia, sensory neglect, and defective access to conscious experience. Neurology. 1991 May;41(5):650–2. http://dx.doi.org/10.1212/WNL.41.5.650 PubMed

28. Verdon V, Schwartz S, Lovblad KO, Hauert CA, Vuilleumier P. Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. Brain. 2010 Mar;133(Pt 3):880–94. http://dx.doi.org/10.1093/brain/awp305 PubMed

29. Gammeri R, Iacono C, Ricci R, Salatino A. Unilateral Spatial Neglect After Stroke: current Insights. Neuropsychiatr Dis Treat. 2020 Jan;16:131–52. http://dx.doi.org/10.2147/NDT.S171461 PubMed

30. Vuilleumier P, Sergent C, Schwartz S, Valenza N, Girardi M, Husain M Impaired perceptual memory of locations across gaze-shifts in patients with unilateral spatial neglect. J Cogn Neurosci. 2007 Aug;19(8):1388–406. http://dx.doi.org/10.1162/jocn.2007.19.8.1388 PubMed

31. Shafer-Skelton A, Kupitz CN, Golomb JD. Object-location binding across a saccade: A retinotopic spatial congruency bias. Atten Percept Psychophys. 2017 Apr;79(3):765–81. http://dx.doi.org/10.3758/s13414-016-1263-8 PubMed

32. Zebhauser PT, Vernet M, Unterburger E, Brem AK. Visuospatial neglect-a theory-informed overview of current and emerging strategies and a systematic review on the therapeutic use of non-invasive brain stimulation. Neuropsychol Rev. 2019 Dec;29(4):397–420. http://dx.doi.org/10.1007/s11065-019-09417-4 PubMed

33. Azouvi P, Samuel C, Louis-Dreyfus A, Bernati T, Bartolomeo P, Beis JM, French Collaborative Study Group on Assessment of Unilateral Neglect (GEREN/GRECO). Sensitivity of clinical and behavioural tests of spatial neglect after right hemisphere stroke. J Neurol Neurosurg Psychiatry. 2002 Aug;73(2):160–6. http://dx.doi.org/10.1136/jnnp.73.2.160 PubMed

34. Lunven M, Bartolomeo P. Attention and spatial cognition: neural and anatomical substrates of visual neglect. Ann Phys Rehabil Med. 2017 Jun;60(3):124–9. http://dx.doi.org/10.1016/j.rehab.2016.01.004 PubMed

35. Mesulam MM. Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos Trans R Soc Lond B Biol Sci. 1999 Jul;354(1387):1325–46. http://dx.doi.org/10.1098/rstb.1999.0482 PubMed

36. Mesulam M. 2.1 Functional anatomy of attention and neglect: from neurons to networks. The cognitive and neural bases of spatial neglect. 2002:33.

37. Buxbaum LJ, Ferraro MK, Veramonti T, Farne A, Whyte J, Ladavas E Hemispatial neglect: Subtypes, neuroanatomy, and disability. Neurology. 2004 Mar;62(5):749–56. http://dx.doi.org/10.1212/01.WNL.0000113730.73031.F4 PubMed

38. Vallar G, Calzolari E. Unilateral spatial neglect after posterior parietal damage. Handb Clin Neurol. 2018;151:287–312. http://dx.doi.org/10.1016/B978-0-444-63622-5.00014-0 PubMed

39. Galletta EE, Campanelli L, Maul KK, Barrett AM. Assessment of neglect dyslexia with functional reading materials. Top Stroke Rehabil. 2014 Jan-Feb;21(1):75–86. http://dx.doi.org/10.1310/tsr2101-75 PubMed

40. Kwon S, Park W, Kim M, Kim JM. Relationship Between Line Bisection Test Time and Hemispatial Neglect Prognosis in Patients With Stroke: A Prospective Pilot Study. Ann Rehabil Med. 2020 Aug;44(4):292–300. http://dx.doi.org/10.5535/arm.19112 PubMed

41. Bailey MJ, Riddoch MJ, Crome P. Evaluation of a test battery for hemineglect in elderly stroke patients for use by therapists in clinical practice. NeuroRehabilitation. 2000;14(3):139–50. http://dx.doi.org/10.3233/NRE-2000-14303 PubMed

42. Schenkenberg T, Bradford DC, Ajax ET. Line bisection and unilateral visual neglect in patients with neurologic impairment. Neurology. 1980 May;30(5):509–17. http://dx.doi.org/10.1212/WNL.30.5.509 PubMed

43. Bisiach E, Bulgarelli C, Sterzi R, Vallar G. Line bisection and cognitive plasticity of unilateral neglect of space. Brain Cogn. 1983 Jan;2(1):32–8. http://dx.doi.org/10.1016/0278-2626(83)90027-1 PubMed

44. Vallar G, Daini R, Antonucci G. Processing of illusion of length in spatial hemineglect: a study of line bisection. Neuropsychologia. 2000;38(7):1087–97. http://dx.doi.org/10.1016/S0028-3932(99)00139-6 PubMed

45. Harvey M, Krämer-McCaffery T, Dow L, Murphy PJ, Gilchrist ID. Categorisation of ‘perceptual’ and ‘premotor’ neglect patients across different tasks: is there strong evidence for a dichotomy? Neuropsychologia. 2002;40(8):1387–95. http://dx.doi.org/10.1016/S0028-3932(01)00202-0 PubMed

46. Milner AD, Harvey M, Roberts RC, Forster SV. Line bisection errors in visual neglect: misguided action or size distortion? Neuropsychologia. 1993 Jan;31(1):39–49. http://dx.doi.org/10.1016/0028-3932(93)90079-F PubMed

47. Vallar G, Mancini F. Mapping the neglect syndrome onto neurofunctional streams. Perception, action, and consciousness. Sensorimotor dynamics and two visual systems. 2010 Aug 19:183-215.

48. Chechlacz M, Rotshtein P, Hansen PC, Deb S, Riddoch MJ, Humphreys GW. The central role of the temporo-parietal junction and the superior longitudinal fasciculus in supporting multi-item competition: evidence from lesion-symptom mapping of extinction. Cortex. 2013 Feb;49(2):487–506. http://dx.doi.org/10.1016/j.cortex.2011.11.008 PubMed

49. Conner AK, Glenn C, Burks JD, McCoy T, Bonney PA, Chema AA The use of the target cancellation task to identify eloquent visuospatial regions in awake craniotomies. Cureus. 2016 Nov;8(11):e883. http://dx.doi.org/10.7759/cureus.883 PubMed

50. Husain M, Kennard C. Distractor-dependent frontal neglect. Neuropsychologia. 1997 Jun;35(6):829–41. http://dx.doi.org/10.1016/S0028-3932(97)00034-1 PubMed

51. Cristinzio C, Bourlon C, Pradat-Diehl P, Trojano L, Grossi D, Chokron S Representational neglect in “invisible” drawing from memory. Cortex. 2009 Mar;45(3):313–7. http://dx.doi.org/10.1016/j.cortex.2008.03.013 PubMed

52. Liu GT, Bolton AK, Price BH, Weintraub S. Dissociated perceptual-sensory and exploratory-motor neglect. J Neurol Neurosurg Psychiatry. 1992 Aug;55(8):701–6. http://dx.doi.org/10.1136/jnnp.55.8.701 PubMed

53. Corbetta M, Shulman GL. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 2002 Mar;3(3):201–15. http://dx.doi.org/10.1038/nrn755 PubMed

54. Gauthier L, Dehaut F, Joanette Y. The bells test: a quantitative and qualitative test for visual neglect. Int J Clin Neuropsychol. 1989 Jan;11(2):49–54.

55. Demeyere N, Riddoch MJ, Slavkova ED, Bickerton WL, Humphreys GW. The Oxford Cognitive Screen (OCS): validation of a stroke-specific short cognitive screening tool. Psychol Assess. 2015 Sep;27(3):883–94. http://dx.doi.org/10.1037/pas0000082 PubMed

56. Ota H, Fujii T, Suzuki K, Fukatsu R, Yamadori A. Dissociation of body-centered and stimulus-centered representations in unilateral neglect. Neurology. 2001 Dec;57(11):2064–9. http://dx.doi.org/10.1212/WNL.57.11.2064 PubMed

57. Ota H, Fujii T, Tabuchi M, Sato K, Saito J, Yamadori A. Different spatial processing for stimulus-centered and body-centered representations. Neurology. 2003 Jun;60(11):1846–8. http://dx.doi.org/10.1212/01.WNL.0000065899.22903.07 PubMed

58. Albert ML. A simple test of visual neglect. Neurology. 1973 Jun;23(6):658–64. http://dx.doi.org/10.1212/WNL.23.6.658 PubMed

59. Sarri M, Greenwood R, Kalra L, Driver J. Task-related modulation of visual neglect in cancellation tasks. Neuropsychologia. 2009 Jan;47(1):91–103. http://dx.doi.org/10.1016/j.neuropsychologia.2008.08.020 PubMed

60. Pedrazzini E, Schnider A, Ptak R. A neuroanatomical model of space-based and object-centered processing in spatial neglect. Brain Struct Funct. 2017 Nov;222(8):3605–13. http://dx.doi.org/10.1007/s00429-017-1420-4 PubMed

61. Shah PP, Spaldo N, Barrett AM, Chen P. Assessment and functional impact of allocentric neglect: a reminder from a case study. Clin Neuropsychol. 2013;27(5):840–63. http://dx.doi.org/10.1080/13854046.2013.783120 PubMed

62. Stone A, Cooke D, Morton D, Steele M. Reliability of revised scoring methods for the Schenkenberg Line Bisection Test with adults following stroke: preliminary findings. Br J Occup Ther. 2019 Dec;82(12):750–8. http://dx.doi.org/10.1177/0308022619866377

63. Vaes N, Lafosse C, Nys G, Schevernels H, Dereymaeker L, Oostra K Capturing peripersonal spatial neglect: an electronic method to quantify visuospatial processes. Behav Res Methods. 2015 Mar;47(1):27–44. http://dx.doi.org/10.3758/s13428-014-0448-0 PubMed

64. Vallar G, Maravita A. Personal and extrapersonal spatial perception.

65. Kleinman JT, Newhart M, Davis C, Heidler-Gary J, Gottesman RF, Hillis AE. Right hemispatial neglect: frequency and characterization following acute left hemisphere stroke. Brain Cogn. 2007 Jun;64(1):50–9. http://dx.doi.org/10.1016/j.bandc.2006.10.005 PubMed

66. Marsh EB, Hillis AE. Dissociation between egocentric and allocentric visuospatial and tactile neglect in acute stroke. Cortex. 2008 Oct;44(9):1215–20. http://dx.doi.org/10.1016/j.cortex.2006.02.002 PubMed

67. Humphreys GW, Gillebert CR, Chechlacz M, Riddoch MJ. Reference frames in visual selection. Ann N Y Acad Sci. 2013 Aug;1296(1):75–87. http://dx.doi.org/10.1111/nyas.12256 PubMed

68. Filimon F. Are all spatial reference frames egocentric? Reinterpreting evidence for allocentric, object-centered, or world-centered reference frames. Front Hum Neurosci. 2015 Dec;9:648. http://dx.doi.org/10.3389/fnhum.2015.00648 PubMed

69. Molenberghs P, Sale MV, Mattingley JB. Is there a critical lesion site for unilateral spatial neglect? A meta-analysis using activation likelihood estimation. Front Hum Neurosci. 2012 Apr;6:78. http://dx.doi.org/10.3389/fnhum.2012.00078 PubMed

70. Lee BH, Suh MK, Kim EJ, Seo SW, Choi KM, Kim GM Neglect dyslexia: frequency, association with other hemispatial neglects, and lesion localization. Neuropsychologia. 2009 Feb;47(3):704–10. http://dx.doi.org/10.1016/j.neuropsychologia.2008.11.027 PubMed

71. Ptak R, Di Pietro M, Schnider A. The neural correlates of object-centered processing in reading: a lesion study of neglect dyslexia. Neuropsychologia. 2012 May;50(6):1142–50. http://dx.doi.org/10.1016/j.neuropsychologia.2011.09.036 PubMed

72. Zacks JM. Neuroimaging studies of mental rotation: a meta-analysis and review. J Cogn Neurosci. 2008 Jan;20(1):1–19. http://dx.doi.org/10.1162/jocn.2008.20013 PubMed

73. Chechlacz M, Rotshtein P, Humphreys GW. Neuroanatomical dissections of unilateral visual neglect symptoms: ALE meta-analysis of lesion-symptom mapping. Front Hum Neurosci. 2012 Aug;6:230. http://dx.doi.org/10.3389/fnhum.2012.00230 PubMed

74. Driver J, Halligan PW. Can visual neglect operate in object-centred co-ordinates? An affirmative single-case study. Cogn Neuropsychol. 1991 Nov;8(6):475–96. http://dx.doi.org/10.1080/02643299108253384

75. Bickerton WL, Samson D, Williamson J, Humphreys GW. Separating forms of neglect using the Apples Test: validation and functional prediction in chronic and acute stroke. Neuropsychology. 2011 Sep;25(5):567–80. http://dx.doi.org/10.1037/a0023501 PubMed

76. Jang SH, Jang WH. The different association of allocentric and egocentric neglect with dorsal and ventral pathways: A case report. Medicine (Baltimore). 2018 Sep;97(37):e12394. http://dx.doi.org/10.1097/MD.0000000000012394 PubMed

78. Hillis AE, Newhart M, Heidler J, Barker PB, Herskovits EH, Degaonkar M. Anatomy of spatial attention: insights from perfusion imaging and hemispatial neglect in acute stroke. J Neurosci. 2005 Mar;25(12):3161–7. http://dx.doi.org/10.1523/JNEUROSCI.4468-04.2005 PubMed

79. Medina J, Kannan V, Pawlak MA, Kleinman JT, Newhart M, Davis C Neural substrates of visuospatial processing in distinct reference frames: evidence from unilateral spatial neglect. J Cogn Neurosci. 2009 Nov;21(11):2073–84. http://dx.doi.org/10.1162/jocn.2008.21160 PubMed

80. Hillis AE. Neurobiology of unilateral spatial neglect. Neuroscientist. 2006 Apr;12(2):153–63. http://dx.doi.org/10.1177/1073858405284257 PubMed

81. Chatterjee A. Picturing unilateral spatial neglect: viewer versus object centred reference frames. J Neurol Neurosurg Psychiatry. 1994 Oct;57(10):1236–40. http://dx.doi.org/10.1136/jnnp.57.10.1236 PubMed

82. Golay L, Schnider A, Ptak R. Cortical and subcortical anatomy of chronic spatial neglect following vascular damage. Behav Brain Funct. 2008 Sep;4(1):43. http://dx.doi.org/10.1186/1744-9081-4-43 PubMed

83. Falchook AD, Mody MD, Srivastava AB, Williamson JB, Heilman KM. Vertical line quadrisection: “what” it represents and who gets the upper hand. Brain Lang. 2013 Nov;127(2):284–8. http://dx.doi.org/10.1016/j.bandl.2012.11.003 PubMed

84. Frassinetti F, Angeli V, Meneghello F, Avanzi S, Làdavas E. Long-lasting amelioration of visuospatial neglect by prism adaptation. Brain. 2002 Mar;125(Pt 3):608–23. http://dx.doi.org/10.1093/brain/awf056 PubMed

85. Rabuffetti M, Farina E, Alberoni M, Pellegatta D, Appollonio I, Affanni P Spatio-temporal features of visual exploration in unilaterally brain-damaged subjects with or without neglect: results from a touchscreen test. PLoS One. 2012;7(2):e31511. http://dx.doi.org/10.1371/journal.pone.0031511 PubMed

86. Pedroli E, Serino S, Cipresso P, Pallavicini F, Riva G. Assessment and rehabilitation of neglect using virtual reality: a systematic review. Front Behav Neurosci. 2015 Aug;9:226. http://dx.doi.org/10.3389/fnbeh.2015.00226 PubMed

87. Kim YM, Chun MH, Yun GJ, Song YJ, Young HE. The effect of virtual reality training on unilateral spatial neglect in stroke patients. Ann Rehabil Med. 2011 Jun;35(3):309–15. http://dx.doi.org/10.5535/arm.2011.35.3.309 PubMed

88. Mainetti R, Sedda A, Ronchetti M, Bottini G, Borghese NA. Duckneglect: video-games based neglect rehabilitation. Technol Health Care. 2013;21(2):97–111. http://dx.doi.org/10.3233/THC-120712 PubMed

89. Fordell H, Bodin K, Eklund A, Malm J. RehAtt - scanning training for neglect enhanced by multi-sensory stimulation in Virtual Reality. Top Stroke Rehabil. 2016 Jun;23(3):191–9. http://dx.doi.org/10.1080/10749357.2016.1138670 PubMed

90. Gammeri R, Turri F, Ricci R, Ptak R. Adaptation to virtual prisms and its relevance for neglect rehabilitation: a single-blind dose-response study with healthy participants. Neuropsychol Rehabil. 2020; 30(4);753-66. PubMed

91. Rose NS, Rendell PG, Hering A, Kliegel M, Bidelman GM, Craik FI. Cognitive and neural plasticity in older adults’ prospective memory following training with the Virtual Week computer game. Front Hum Neurosci. 2015 Oct;9:592. http://dx.doi.org/10.3389/fnhum.2015.00592 PubMed

92. Black RD, Rogers LL, Ade KK, Nicoletto HA, Adkins HD, Laskowitz DT. Non-invasive neuromodulation using time-varying caloric vestibular stimulation. IEEE J Transl Eng Health Med. 2016 Oct;4:2000310. http://dx.doi.org/10.1109/JTEHM.2016.2615899 PubMed

93. Cazzoli D, Müri RM, Schumacher R, von Arx S, Chaves S, Gutbrod K Theta burst stimulation reduces disability during the activities of daily living in spatial neglect. Brain. 2012 Nov;135(Pt 11):3426–39. http://dx.doi.org/10.1093/brain/aws182 PubMed

94. Koch G, Bonnì S, Giacobbe V, Bucchi G, Basile B, Lupo F θ-burst stimulation of the left hemisphere accelerates recovery of hemispatial neglect. Neurology. 2012 Jan;78(1):24–30. http://dx.doi.org/10.1212/WNL.0b013e31823ed08f PubMed

95. Di Gregorio F, La Porta F, Casanova E, Magni E, Bonora R, Ercolino MG Efficacy of repetitive transcranial magnetic stimulation combined with visual scanning treatment on cognitive and behavioral symptoms of left hemispatial neglect in right hemispheric stroke patients: study protocol for a randomized controlled trial. Trials. 2021 Jan;22(1):24. http://dx.doi.org/10.1186/s13063-020-04943-6 PubMed

96. Brem AK, Unterburger E, Speight I, Jäncke L. Treatment of visuospatial neglect with biparietal tDCS and cognitive training: a single-case study. Front Syst Neurosci. 2014 Sep;8:180. http://dx.doi.org/10.3389/fnsys.2014.00180 PubMed

97. Yi YG, Chun MH, Do KH, Sung EJ, Kwon YG, Kim DY. The effect of transcranial direct current stimulation on neglect syndrome in stroke patients. Ann Rehabil Med. 2016 Apr;40(2):223–9. http://dx.doi.org/10.5535/arm.2016.40.2.223 PubMed

98. Turgut N, Miranda M, Kastrup A, Eling P, Hildebrandt H. tDCS combined with optokinetic drift reduces egocentric neglect in severely impaired post-acute patients. Neuropsychol Rehabil. 2018 Jun;28(4):515–26. http://dx.doi.org/10.1080/09602011.2016.1202120 PubMed

99. Vaes N, Nys G, Lafosse C, Dereymaeker L, Oostra K, Hemelsoet D Rehabilitation of visuospatial neglect by prism adaptation: effects of a mild treatment regime. A randomised controlled trial. Neuropsychol Rehabil. 2018 Sep;28(6):899–918. http://dx.doi.org/10.1080/09602011.2016.1208617 PubMed

100. Rousseaux M, Bernati T, Saj A, Kozlowski O. Ineffectiveness of prism adaptation on spatial neglect signs. Stroke. 2006 Feb;37(2):542–3. http://dx.doi.org/10.1161/01.STR.0000198877.09270.e8 PubMed

101. Ten Brink AF, Visser-Meily JM, Schut MJ, Kouwenhoven M, Eijsackers AL, Nijboer TC. Prism adaptation in rehabilitation? No additional effects of prism adaptation on neglect recovery in the subacute phase poststroke: A randomized controlled trial. Neurorehabil Neural Repair. 2017 Dec;31(12):1017–28. http://dx.doi.org/10.1177/1545968317744277 PubMed

102. Saj A, Pierce J, Caroli A, Ronchi R, Thomasson M, Vuilleumier P. Rightward exogenous attentional shifts impair perceptual memory of spatial locations in patients with left unilateral spatial neglect. Cortex. 2020 Jan;122:187–97. http://dx.doi.org/10.1016/j.cortex.2019.10.002 PubMed

103. Saj A, Cojan Y, Assal F, Vuilleumier P. Prism adaptation effect on neural activity and spatial neglect depend on brain lesion site. Cortex. 2019 Oct;119:301–11. http://dx.doi.org/10.1016/j.cortex.2019.04.022 PubMed

104. Saj A, Pierce JE, Ronchi R, Ros T, Thomasson M, Bernati T Real-time fMRI and EEG neurofeedback: A perspective on applications for the rehabilitation of spatial neglect. Ann Phys Rehabil Med. 2021 Sep;64(5):101561. http://dx.doi.org/10.1016/j.rehab.2021.101561 PubMed

105. Robineau F, Saj A, Neveu R, Van De Ville D, Scharnowski F, Vuilleumier P. Using real-time fMRI neurofeedback to restore right occipital cortex activity in patients with left visuo-spatial neglect: proof-of-principle and preliminary results. Neuropsychol Rehabil. 2019 Apr;29(3):339–60. http://dx.doi.org/10.1080/09602011.2017.1301262 PubMed

106. Goodglass H, Kaplan E. The Assessment of Aphasia and Related Disorders, 2nd edn Lea & Febiger: Philadelphia. Dictionary of Biological Psychology. 1983;230.

107. Stone SP, Wilson B, Wroot A, Halligan PW, Lange LS, Marshall JC The assessment of visuo-spatial neglect after acute stroke. J Neurol Neurosurg Psychiatry. 1991 Apr;54(4):345–50. http://dx.doi.org/10.1136/jnnp.54.4.345 PubMed

108. Nyffeler T, Paladini RE, Hopfner S, Job O, Nef T, Pflugshaupt T Contralesional trunk rotation dissociates real vs. pseudo-visual field defects due to visual neglect in stroke patients. Front Neurol. 2017 Aug;8:411. http://dx.doi.org/10.3389/fneur.2017.00411 PubMed

109. Kaufmann BC, Cazzoli D, Pflugshaupt T, Bohlhalter S, Vanbellingen T, Müri RM Eyetracking during free visual exploration detects neglect more reliably than paper-pencil tests. Cortex. 2020 Aug;129:223–35. http://dx.doi.org/10.1016/j.cortex.2020.04.021 PubMed

110. Reinhart S, Leonhard E, Kerkhoff G. SNT-single und SNT-dual: zwei neue sensitive Neglecttests für den leichten und chronischen Neglect. NeuroRehabilitation. 2016;22(1):98–104.

111. Stone SP, Halligan PW, Greenwood RJ. The incidence of neglect phenomena and related disorders in patients with an acute right or left hemisphere stroke. Age Ageing. 1993 Jan;22(1):46–52. http://dx.doi.org/10.1093/ageing/22.1.46 PubMed

112. Siekierka-Kleiser EM, Kleiser R, Wohlschläger AM, Freund HJ, Seitz RJ. Quantitative assessment of recovery from motor hemineglect in acute stroke patients. Cerebrovasc Dis. 2006;21(5-6):307–14. http://dx.doi.org/10.1159/000091535 PubMed

113. Bisiach E, Luzzatti C. Unilateral neglect of representational space. Cortex. 1978 Mar;14(1):129–33. http://dx.doi.org/10.1016/S0010-9452(78)80016-1 PubMed

114. Bellmann A, Meuli R, Clarke S. Two types of auditory neglect. Brain. 2001 Apr;124(Pt 4):676–87. http://dx.doi.org/10.1093/brain/124.4.676 PubMed

115. Gokhale S, Lahoti S, Caplan LR. The neglected neglect: auditory neglect. JAMA Neurol. 2013 Aug;70(8):1065–9. http://dx.doi.org/10.1001/jamaneurol.2013.155 PubMed

116. Husain M, Mannan S, Hodgson T, Wojciulik E, Driver J, Kennard C. Impaired spatial working memory across saccades contributes to abnormal search in parietal neglect. Brain. 2001 May;124(Pt 5):941–52. http://dx.doi.org/10.1093/brain/124.5.941 PubMed

117. Ogourtsova T, Archambault P, Sangani S, Lamontagne A. Ecological Virtual Reality Evaluation of Neglect Symptoms (EVENS): effects of virtual scene complexity in the assessment of poststroke unilateral spatial neglect. Neurorehabil Neural Repair. 2018 Jan;32(1):46–61. http://dx.doi.org/10.1177/1545968317751677 PubMed

118. Wager TD, Smith EE. Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci. 2003 Dec;3(4):255–74. http://dx.doi.org/10.3758/CABN.3.4.255 PubMed

119. Laplane D, Baulac M, Carydakis C. [Motor neglect of thalamic origin]. Rev Neurol (Paris). 1986;142(4):375–9. PubMed

120. Chamorro A, Marshall RS, Valls-Solé J, Tolosa E, Mohr JP. Motor behavior in stroke patients with isolated medial frontal ischemic infarction. Stroke. 1997 Sep;28(9):1755–60. http://dx.doi.org/10.1161/01.STR.28.9.1755 PubMed

121. Kaufmann BC, Cazzoli D, Pflugshaupt T, Bohlhalter S, Vanbellingen T, Müri RM Eyetracking during free visual exploration detects neglect more reliably than paper-pencil tests. Cortex. 2020 Aug;129:223–35. http://dx.doi.org/10.1016/j.cortex.2020.04.021 PubMed

122. Knobel SE, Kaufmann BC, Gerber SM, Urwyler P, Cazzoli D, Müri RM Development of a Search Task Using Immersive Virtual Reality: Proof-of-Concept Study. JMIR Serious Games. 2021 Jul;9(3):e29182. http://dx.doi.org/10.2196/29182 PubMed

123. Müri RM, Cazzoli D, Nef T, Mosimann UP, Hopfner S, Nyffeler T. Non-invasive brain stimulation in neglect rehabilitation: an update. Front Hum Neurosci. 2013 Jun;7:248. http://dx.doi.org/10.3389/fnhum.2013.00248 PubMed

124. Koch G, Bonnì S, Giacobbe V, Bucchi G, Basile B, Lupo F θ-burst stimulation of the left hemisphere accelerates recovery of hemispatial neglect. Neurology. 2012 Jan;78(1):24–30. http://dx.doi.org/10.1212/WNL.0b013e31823ed08f PubMed

125. Nyffeler T, Cazzoli D, Hess CW, Müri RM. One session of repeated parietal theta burst stimulation trains induces long-lasting improvement of visual neglect. Stroke. 2009 Aug;40(8):2791–6. http://dx.doi.org/10.1161/STROKEAHA.109.552323 PubMed

126. Nyffeler T, Vanbellingen T, Kaufmann BC, Pflugshaupt T, Bauer D, Frey J Theta burst stimulation in neglect after stroke: functional outcome and response variability origins. Brain. 2019 Apr;142(4):992–1008. http://dx.doi.org/10.1093/brain/awz029 PubMed

127. Kerkhoff G, Keller I, Artinger F, Hildebrandt H, Marquardt C, Reinhart S Recovery from auditory and visual neglect after optokinetic stimulation with pursuit eye movements—transient modulation and enduring treatment effects. Neuropsychologia. 2012 May;50(6):1164–77. http://dx.doi.org/10.1016/j.neuropsychologia.2011.09.032 PubMed

128. Ronchi R, Perez-Marcos D, Giroux A, Thomasson M, Serino A, Saj A Use of immersive virtual reality to detect unilateral spatial neglect in chronic stroke. Ann Phys Rehabil Med. 2018;61:e90–1. http://dx.doi.org/10.1016/j.rehab.2018.05.193

129. Ros T, Michela A, Mayer A, Bellmann A, Vuadens P, Zermatten V Disruption of large-scale electrophysiological networks in stroke patients with visuospatial neglect. Netw Neurosci. 2022 Feb;6(1):69–89. http://dx.doi.org/10.1162/netn_a_00210 PubMed

130. Kocanaogullari D, Mak J, Kersey J, Khalaf A, Ostadabbas S, Wittenberg G EEG-based Neglect Detection for Stroke Patients. Annu Int Conf IEEE Eng Med Biol Soc. 2020 Jul;2020:264–7. PubMed

131. Binder J, Marshall R, Lazar R, Benjamin J, Mohr JP. Distinct syndromes of hemineglect. Arch Neurol. 1992 Nov;49(11):1187–94. http://dx.doi.org/10.1001/archneur.1992.00530350109026 PubMed

132. Rorden C, Karnath HO. A simple measure of neglect severity. Neuropsychologia. 2010 Jul;48(9):2758–63. http://dx.doi.org/10.1016/j.neuropsychologia.2010.04.018 PubMed

Verpassen Sie keinen Artikel!

close